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Protistology Fine Structure of Nucleoli in the Ciliate Didinium Nasutum*

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Protistology Fine Structure of Nucleoli in the Ciliate Didinium Nasutum* Protistology 3 (2), 99-106 (2003) Protistology Fine structure of nucleoli in the ciliate Didinium nasutum* Bella P. Karajan1, Vladimir I. Popenko2 and Olga G. Leonova2 1 Institute of Cytology, Russian Academy of Sciences, 4 Tikhoretsky Avenue, 194064 St. Petersburg, Russia 2 Institute of Molecular Biology, Russian Academy of Sciences, 32 Vavilov Street, 119991 Moscow, Russia Summary The macronuclear nucleoli of vegetative non-dividing cells of Didinium nasutum display inverted position of the main parts: the granular component is inside and the dense fibrillar one, in form of discrete bands, is mainly at the periphery. Before binary fission, the nucleoli are degranulated and their fibrillar bands scatter throughout the macronucleus, to be segregated during division between the daughter cells, where they begin to re-form the granular parts. In young resting cysts small nucleoli consist of granular material only, larger nucleoli show a clear segregation of its fibrillar and granular elements. During conjugation, nucleoli of the old macronucleus or of its fragments become segregated into granular and fibrillar parts and the latter are largely eliminated. The nucleoli lose contact with the chromatin bodies. In the developing anlagen of the new macronuclei the first nucleoli appear as fibrous bodies and only later develop granular parts; simultaneously the number of nucleoli increases. Key Words: macronucleus, nucleoli, cell cycle, cysts, Didinium nasutum 1995). The organization of rDNA in gymnostomes, Introduction including Didinium, is not known yet. The macronuclear nucleoli can fuse, separate, Macronuclear nucleoli are known to be very labile segregate into granular and fibrillar parts, or become structures. In all known cases, they are formed on degranulated depending on various environmental extrachromosomal (amplified) copies of ribosomal RNA factors, clonal growth phase, nutritional state, cell cycle gene sequence, the so-called rDNA, which may be period, encystment, conjugation and so on (Raikov, monomeric, as in Glaucoma and all hypotrichs, dimeric 1982, 1995). These changes may occur on the repli- palindromic, as in Tetrahymena or oligomeric as in cation level (i.e., via change of the copy number of the Paramecium (Blackburn, 1982; Raikov, 1982, 1989, rDNA due to differential replication of the amplified extrachromosomal rDNA) or on the transcription level * In memory of Professor Igor Borisovich Raikov (i.e., due to differences in the rate of preribosomal RNA (30.12.1932-27.10.1998) synthesis), or else on the posttranscriptional level (i.e., © 2003 by Russia, Protistology 100 · Bella P. Karajan, Vladimir I. Popenko and Olga G. Leonova due to differences in the rate of rRNA processing and maturation of ribosomal particles). This paper aims to follow the fine structural changes of nucleoli at various stages of cell cycle of Didmium nasutum. Material and methods The laboratory strain of Didinium nasutum used in the present work has been cultivated at room tempe- rature in lettuce medium and fed with Paramecium caudatum cultivated separately. The following fixation schedules were used: 1) 2% osmium tetroxyde in a 0.05 M sodium cacodylate buffer (pH 7.2), 30 min on ice. 2) A freshly prepared mixture of glutaraldehyde and osmium tetroxyde with the following final concen- trations: glutaraldehyde, 1%; osmium tetroxyde, 1%; phosphate buffer, pH 7.2, 0,05 M. Fix 30 min to 1 h on ice and in the darkness. The sections were routinely stained and studied with a JEM-100C electron microscope operated at 80 kv. Results VEGETATIVE CELL AND BINNARY FISSION The macronucleus of normally fed interphase cells contains numerous rather conspicuous nucleoli. The nucleoli show an inverted disposition of its main components: the dense fibrillar component mainly occurs in form of discrete bands at the surface of the nucleoli and around intranucleolar chromatin bodies, and the granular component lies inside the nucleoli. The nucleolar organizers in form of compact chromatin bodies either lie inside the nucleoli, surrounded by a ring of dense fibrillar bands, or at the surface, where they also contact bands of the dense fibrillar component (Fig. 1A). The latter bodies are indistinguishable from “free’’ chromatin bodies (see: Karadzhan and Raikov, 1977). Chromatin bodies, both intranucleolar and peripheral, often decondense forming fibrillar centres (NORs) as defined by Goessens (1974). When the macronucleus prepares to divide, it contracts from a horseshoe shape to a more or less rounded one and then begins stretching in a rod. During the stretching phase, numerous bundles of longitudinal microtubules assemble in the macronucleus. The nucleoli become largely degranulated and the dense fibrillar bands Fig. 1. Nucleoli in the interphase (А) and in a dividing become free and scatter throughout the macronucleus macronucleus (B, C). Abbreviations: c- chromatin during the contraction phase; their contacts with bodies, f - fibrillar component of the nucleolus, g - chromatin bodies are no more evident (Fig. 1B). The granular component of the nucleolus, inc - intra- general disposition of the nucleolar remnants is nucleolar chromatin body, n - nucleoli. Scale bars: reminiscent of a swirling movement described during pre- A, C - 0,5 µm, B - 1 µm. Protistology · 101 Fig. 2. Nucleoli in a young resting cyst. A - a general view of the macronucleus of a young cyst. The small granular nucleoli are designated by arrows. B - a relatively large nucleolus shown in A, at higher magnification. C - a small granular nucleolus (arrow) at higher magnification. Abbreviations: ln - a relatively large nucleolus (~ 800 nm in size) with segregated fibrillar and granular components, other abbreviations are the same as in Fig. 1. Scale bars: A - 1 µm, B, C - 0,2 µm. divisional contraction of the macronucleus in several considerably. Larger nucleoli show a clear segregation of ciliates (Raikov, 1982). fibrillar and granular component, but the segregation of During the stretching phase and the actual division the nucleolar component in young resting cysts obviously (pinching in two), the granular nucleolar component proceeds differently from that observed in the fragments begins to re-appear, but it is not yet organized into of old macronucleus during conjugation. The fibrillar regular nucleoli (Fig. 1C). The nucleolar material is component in this case is immersed in a granular mass of caught between microtubule bundles, the dense fibrillar the nucleolus (Fig. 2B). The small nucleoli consist of bands are mostly isolated and have the same longi- granular material only (Fig. 2C). Nucleolar organizers, tudinal orientation as microtubules (Fig. 1C). However, both inter- and perinucleolar, are not observed. the contact between chromatin bodies and fibrillar bands is re-established. All this argues for that the OLD MACRONUCLEUS DURING CONJUGATION biosynthetic activity of the nucleoli is resumed. During the first meiotic division of the micronucleus (2-3 h after the start of conjugation), the old macronucleus CYSTS fragments into 20-30 pieces (Karadzhan and Raikov, Cells of Didinium nasutum can differentiate into 1979). Each piece usually contains several nucleoli. During resting cysts under unfavorable condition, such as the second meiotic division the peripheral position of the starvation, temperature stress and so on. We have bands of the dense fibrillar nucleolar component becomes investigated the young resting cysts, less than 16 h old, clearer than in vegetative cells; intranucleolar chromatin which formed spontaneously in a somewhat inhibited bodies disappear and the connection of the main culture. chromatin mass with the nucleoli is lost (Fig. 3A). This Number of nucleoli as well as the size of single can be considered as the onset of nucleolar segregation nucleoli in resting cysts reduce drastically (Fig. 2A). The into the fibrillar and the granular components. size of each nucleolus remains within the limits of 150 Somewhat later, usually still during the 2nd meiotic to 900 nm. The structure of nucleoli also changes division, the peripheral fibrillar bands contract and 102 · Bella P. Karajan, Vladimir I. Popenko and Olga G. Leonova coalesce into compact blocks (Fig. 3B). The rest of the bodies which depress the nucleolar surface (Fig. 3E). These nucleoli is granular. Nucleolar organizers, both intra- would enter the nucleoli and become the intranucleolar and perinucleolar, are absent. chromatin bodies. Simultaneously granular material During the first or the second synkaryon division begins to accumulate inside each nucleolus; additional the chromatin of the macronuclear fragments con- nucleoli are possibly also formed during this time, as their denses into a common spongy mass and at the same number grows. The fibrous bands always remain at the time the envelope of the fragments begins «to peel off» nucleolar surface (Fig. 3E). Sometimes such nucleoli fuse establishing direct contact of the macronuclear forming a large compound one. contents with the cytoplasm (Karadzhan and Raikov, 1979). The nucleoli remain segregated and devoid of Discussion NORs. They are located in holes in the chromatin mass and are always surrounded by a rim of struc- VEGETATIVE MACRONUCLEUS tureless nucleoplasm (Fig. 3C). Possibly the nucleoli give off a part of their granules to the cytoplasm. About In vegetative non-dividing macronuclei the the same time or a little later each macronuclear nucleolar morphology mainly depends on the nutri- fragment, together with some adjacent cytoplasm, tional
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